Differential growth costs and nitrogen fixation in Cytisus multiflorus (L′Hér.) Sweet and Cytisus scoparius (L.) Link are mediated by sources of inorganic N

• Shrubby legumes in Mediterranean‐type ecosystems face strong nutrient limitations that worsen in summer, when water is absent. Nitrogen‐fixing legumes are likely to be able to switch between soil N and atmospheric N (N₂) sources to adjust the C costs of N acquisition in different seasons.
• We investigated the utilisation of different inorganic N sources by two indigenous shrubby legumes (Cytisus multiflorus and Cytisus scoparius). Plant performance in terms of photosynthesis and biomass production was also analysed. Plants were cultivated in sterile river sand supplied with Hoagland nutrient solution, grown in N‐free nutrient solution and inoculated with effective rhizobial strains from nodules of adult plants of the same species. A second treatment consisted of plants given 500 μm NH₄NO₃ added into the nutrient solution. In a third treatment, plants were watered with another source of N (500 μm NH₄NO₃) as well as being inoculated with effective rhizobial strains.
• The application of NH₄NO₃ to the legumes resulted in a larger increase in plant dry matter. Carbon construction costs were higher in plants supplied with mineral and symbiotic N sources and always higher in the endemic C. multiflorus. Differences in photosynthesis rates were only observed between species, regardless of the N source. Non‐fertilised inoculated plants had more effective root nodules and a clear dependence on N₂ fixation.
• We propose that the ability of C. scoparius to change N source makes it a plastic species, which would account for its broader distribution in nature.

     

Loss‐of‐function of ASPARTIC PEPTIDASE NODULE‐INDUCED 1 (APN1) in Lotus japonicus restricts efficient nitrogen‐fixing symbiosis with specific Mesorhizobium loti strains

The nitrogen‐fixing symbiosis of legumes and Rhizobium bacteria is established by complex interactions between the two symbiotic partners. Legume Fix^– mutants form apparently normal nodules with endosymbiotic rhizobia but fail to induce rhizobial nitrogen fixation. These mutants are useful for identifying the legume genes involved in the interactions essential for symbiotic nitrogen fixation. We describe here a Fix^– mutant of Lotus japonicus, apn1, which showed a very specific symbiotic phenotype. It formed ineffective nodules when inoculated with the Mesorhizobium loti strain TONO. In these nodules, infected cells disintegrated and successively became necrotic, indicating premature senescence typical of Fix^– mutants. However, it formed effective nodules when inoculated with the M. loti strain MAFF303099. Among nine different M. loti strains tested, four formed ineffective nodules and five formed effective nodules on apn1 roots. The identified causal gene, ASPARTIC PEPTIDASE NODULE‐INDUCED 1 (LjAPN1), encodes a nepenthesin‐type aspartic peptidase. The well characterized Arabidopsis aspartic peptidase CDR1 could complement the strain‐specific Fix^– phenotype of apn1. LjAPN1 is a typical late nodulin; its gene expression was exclusively induced during nodule development. LjAPN1 was most abundantly expressed in the infected cells in the nodules. Our findings indicate that LjAPN1 is required for the development and persistence of functional (nitrogen‐fixing) symbiosis in a rhizobial strain‐dependent manner, and thus determines compatibility between M. loti and L. japonicus at the level of nitrogen fixation.     

Functional dimorphic enantiostyly in monomorphic enantiostylous species of the subtribe Cassiinae (Fabaceae‐Caesalpinioideae)

• Monomorphic enantiostylous species produce flowers with a displacement of the style to the left (L) or right (R) on the same individual, and may exhibit different dynamics for the production of these floral types, which may influence levels of selfing.
• We investigated the production dynamics of L and R floral types in seven species and a variety of monomorphic enantiostylous species of the genera Senna and Chamaecrista. Our hypothesis was that most species present similar proportions of floral morphs each day. Individuals were classified daily over a period of 7 days according to the functional status, i.e. the proportion of floral morphs as functionally L, R or reciprocal (REC, i.e. similar proportions of the two floral morphs), and also according to the number of consecutive days in which they exhibited the same functional status.
• All species presented low daily flower production. Most species had individuals classified as functionally R, L and REC, and tend to repeat the same functional status over a few days, although they may change functional status during the flowering period. All species exhibited individuals that were classified as functionally reciprocal when both the daily and total number of flowers produced over 7 days was considered. The occurrence of different functional status has not yet been reported in the literature for enantiostylous species.
• The distinct strategies observed in the dynamics of floral morph production seemed likely to minimise geitonogamy and to favour cross‐pollination between individuals (xenogamy).

     

The presence of nodules on legume root systems can alter phenotypic plasticity in response to internal nitrogen independent of nitrogen fixation

All higher plants show developmental plasticity in response to the availability of nitrogen (N) in the soil. In legumes, N starvation causes the formation of root nodules, where symbiotic rhizobacteria fix atmospheric N₂ for the host in exchange for fixed carbon (C) from the shoot. Here, we tested whether plastic responses to internal [N] of legumes are altered by their symbionts. Glasshouse experiments compared root phenotypes of three legumes, Medicago truncatula, Medicago sativa and Trifolium subterraneum, inoculated with their compatible symbiont partners and grown under four nitrate levels. In addition, six strains of rhizobia, differing in their ability to fix N₂ in M. truncatula, were compared to test if plastic responses to internal [N] were dependent on the rhizobia or N₂‐fixing capability of the nodules. We found that the presence of rhizobia affected phenotypic plasticity of the legumes to internal [N], particularly in root length and root mass ratio (RMR), in a plant species‐dependent way. While root length responses of M. truncatula to internal [N] were dependent on the ability of rhizobial symbionts to fix N₂, RMR response to internal [N] was dependent only on initiation of nodules, irrespective of N₂‐fixing ability of the rhizobia strains.     

Orchid seed removal by ants in Neotropical ant‐gardens

• Most plants that inhabit ant‐gardens (AGs) are cultivated by the ants. Some orchids occur in AGs; however, it is not known whether their seeds are dispersed by AG ants because most orchid seeds are tiny and dispersed by wind.
• We performed in situ seed removal experiments, in which we simultaneously provided Azteca gnava ants with seeds of three AG orchid species and three other AG epiphyte species (Bromeliaceae, Cactaceae and Gesneriaceae), as well as the non‐AG orchid Catasetum integerrimum.
• The seeds most removed were those of the bromeliad Aechmea tillandsioides and the gesneriad Codonanthe uleana, while seeds of AG orchids Coryanthes picturata, Epidendrum flexuosum and Epidendrum pachyrachis were less removed. The non‐AG orchid was not removed. Removal values were positively correlated with the frequency of the AG epiphytes in the AGs, and seeds of AG orchids were larger than those of non‐AG orchids, which should favour myrmecochory.
• Our data show that Azt. gnava ants discriminate and preferentially remove seeds of the AG epiphytes. We report for the first time the removal of AG orchid seeds by AG ants in Neotropical AGs.

     

Polyphasic approach for the characterization of rhizobial symbionts effective in fixing N<Subscript>2</Subscript> with common bean (<Emphasis Type="Italic">Phaseolus vulgaris</Emphasis> L.)

Common bean (Phaseolus vulgaris L.) is a legume that has been reported as highly promiscuous in nodulating with a variety of rhizobial strains, often with low effectiveness in fixing nitrogen. The aim of this work was to assess the symbiotic efficiency of rhizobial strains isolated from common bean seeds, nodules of Arachis hypogaea, Mucuna pruriens, and soils from various Brazilian agroecosystems, followed by the characterization of elite strains identified in the first screening. Forty-five elite strains were analyzed for symbiotic properties (nodulation, plant-growth, and nitrogen-fixation parameters) under greenhouse conditions in pots containing non-sterile soil, and variation in symbiotic performance was observed. Elite strains were also characterized in relation to morpho-physiological properties, genetic profiles of rep-polymerase chain reaction (PCR; BOX), and restriction fragment length polymorphism (RFLP)-PCR of the 16S rRNA. Sequence analyses of the 16S rRNA were obtained for 17 strains representative of the main groups resulting from all previous analyses. One of the most effective strains, IPR-Pv 2604, was clustered with Rhizobium tropici, whereas strain IPR-Pv 583, showing lower effectiveness in fixing N₂, was clustered with Herbaspirillum lusitanum. Surprisingly, effective strains were clustered with unusual symbiotic genera/species, including Leifsonia xyli, Stenotrophomonas maltophilia, Burkholderia, and Enterobacter. Some strains recognized in this study were outstanding in their nitrogen-fixing capacity and therefore, show high biotechnological potential for use in commercial inoculants.     

MALDI mass spectrometry‐assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula–Sinorhizobium meliloti symbiosis

Symbiotic associations between leguminous plants and nitrogen‐fixing rhizobia culminate in the formation of specialized organs called root nodules, in which the rhizobia fix atmospheric nitrogen and transfer it to the plant. Efficient biological nitrogen fixation depends on metabolites produced by and exchanged between both partners. The Medicago truncatula–Sinorhizobium meliloti association is an excellent model for dissecting this nitrogen‐fixing symbiosis because of the availability of genetic information for both symbiotic partners. Here, we employed a powerful imaging technique – matrix‐assisted laser desorption/ionization (MALDI)/mass spectrometric imaging (MSI) – to study metabolite distribution in roots and root nodules of M. truncatula during nitrogen fixation. The combination of an efficient, novel MALDI matrix [1,8–bis(dimethyl‐amino) naphthalene, DMAN] with a conventional matrix 2,5–dihydroxybenzoic acid (DHB) allowed detection of a large array of organic acids, amino acids, sugars, lipids, flavonoids and their conjugates with improved coverage. Ion density maps of representative metabolites are presented and correlated with the nitrogen fixation process. We demonstrate differences in metabolite distribution between roots and nodules, and also between fixing and non‐fixing nodules produced by plant and bacterial mutants. Our study highlights the benefits of using MSI for detecting differences in metabolite distributions in plant biology.     

Toxic Microcystis (cyanobacteria) inhibit recruitment of the bloom‐enhancing invasive bivalve Limnoperna fortunei

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Pollen and stigma size changes during the transition from tristyly to distyly in Oxalis alpina (Oxalidaceae)

• Pollen and stigma size have the potential to influence male fitness of hermaphroditic plants, particularly in species presenting floral polymorphisms characterised by marked differences in these traits among floral morphs. In this study, we take advantage of the evolutionary transition from tristyly to distyly experienced by Oxalis alpina (Oxalidaceae), and examined whether modifications in the ancillary traits (pollen and stigma size) respond to allometric changes in other floral traits. Also, we tested whether these modifications are in accordance with what would be expected under the hypothesis that novel competitive scenarios (as in distylous‐derived reproductive system) exert morph‐ and whorl‐specific selective pressures to match the available stigmas.
• We measure pollen and stigma size in five populations of O. alpina representing the tristyly–distyly transition.
• A general reduction in pollen and stigma size occurred along the tristyly–distyly transition, and pollen size from the two anther levels within each morph converged to a similar size that was characterised by whorl‐specific changes (increases or decreases) in pollen size of different anthers in each floral type.
• Overall, results from this study show that the evolution of distyly in this species is characterised not only by changes in sexual organ position and flower size, but also by morph‐specific changes in pollen and stigma size. This evidence supports the importance of selection on pollen and stigma size, which increase fitness of remaining morphs following the evolution of distyly, and raises questions to explore on the functional value of pollen size in heterostylous systems under pollen competition.

     

Impact of pre‐ and post‐pollination barriers on pollen transfer and reproductive isolation among three sympatric Pedicularis (Orobanchaceae) species

• Pedicularis is the largest genus in the Orobanchaceae (>300) with many species co‐occurring and co‐blooming in subalpine to alpine meadows in the Himalayas. Although it is well known that different Pedicularis species place pollen on different parts of the same bumblebee's body, thus reducing interspecific pollen transfer, it is not known whether post‐pollination components also contribute to reproductive isolation (RI).
• In this study, we quantified the individual strengths and absolute contributions of six pre‐ and post‐pollination components of RI between three sympatric species in two pairs; Pedicularis gruina × Pedicularis tenuisecta (gru × ten) and Pedicularis comptoniifolia × Pedicularis tenuisecta (com × ten).
• All three Pedicularis species shared the same Bombus species. Individual foragers showed a high, but incomplete, floral constancy for each species. Therefore, pre‐pollination barriers were potentially ‘leaky’ as Bombus species showed a low but consistent frequency of interspecific visitation. The RI strength of pre‐pollination was lower in com × ten than in gru × ten. In contrast, post‐pollination barriers completely blocked gene flow between both sets of species pairs. Two post‐pollination recognition sites were identified. Late acting rejection of interspecific pollen tube growth occurred in com♀ × ten♂, while seeds produced in bi‐directional crosses of gru × ten failed to germinate.
• We propose that, although floral isolation based on pollen placement on pollinators in the genus Pedicularis is crucial to avoid interspecific pollen transfer, the importance of this mode of interspecific isolation may be exaggerated. Post‐pollination barriers may play even larger roles for currently established populations of co‐blooming and sympatric species in this huge genus in the Himalayas.

     

Laser‐ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia

Technologies enabling in situ metabolic profiling of living plant systems are invaluable for understanding physiological processes and could be used for rapid phenotypic screening (e.g., to produce plants with superior biological nitrogen‐fixing ability). The symbiotic interaction between legumes and nitrogen‐fixing soil bacteria results in a specialized plant organ (i.e., root nodule) where the exchange of nutrients between host and endosymbiont occurs. Laser‐ablation electrospray ionization mass spectrometry (LAESI‐MS) is a method that can be performed under ambient conditions requiring minimal sample preparation. Here, we employed LAESI‐MS to explore the well characterized symbiosis between soybean (Glycine max L. Merr.) and its compatible symbiont, Bradyrhizobium japonicum. The utilization of ion mobility separation (IMS) improved the molecular coverage, selectivity, and identification of the detected biomolecules. Specifically, incorporation of IMS resulted in an increase of 153 differentially abundant spectral features in the nodule samples. The data presented demonstrate the advantages of using LAESI–IMS–MS for the rapid analysis of intact root nodules, uninfected root segments, and free‐living rhizobia. Untargeted pathway analysis revealed several metabolic processes within the nodule (e.g., zeatin, riboflavin, and purine synthesis). Compounds specific to the uninfected root and bacteria were also detected. Lastly, we performed depth profiling of intact nodules to reveal the location of metabolites to the cortex and inside the infected region, and lateral profiling of sectioned nodules confirmed these molecular distributions. Our results established the feasibility of LAESI–IMS–MS for the analysis and spatial mapping of plant tissues, with its specific demonstration to improve our understanding of the soybean‐rhizobial symbiosis.     

Positive co‐occurrence between feeding‐associative savannah fishes depends on species and habitat

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Species‐specific separation of lake plankton reveals divergent food assimilation patterns in rotifers

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Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios

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Mixed pollen load and late‐acting self‐incompatibility flexibility in Adenocalymma peregrinum (Miers) L.G. Lohmann (Bignonieae: Bignoniaceae)

• Mixed cross and self‐pollen load on the stigma (mixed pollination) of species with late‐acting self‐incompatibility system (LSI) can lead to self‐fertilized seed production. This “cryptic self‐fertility” may allow selfed seedling development in species otherwise largely self‐sterile. Our aims were to check if mixed pollinations would lead to fruit set in LSI Adenocalymma peregrinum, and test for evidence of early‐acting inbreeding depression in putative selfed seeds from mixed pollinations.
• Experimental pollinations were carried out in a natural population. Fruit and seed set from self‐, cross and mixed pollinations were analysed. Further germination tests were carried out for the seeds obtained from treatments.
• Our results confirm self‐incompatibility, and fruit set from cross‐pollinations was three‐fold that from mixed pollinations. This low fruit set in mixed pollinations is most likely due to a greater number of self‐ than cross‐fertilized ovules, which promotes LSI action and pistil abortion. Likewise, higher percentage of empty seeds in surviving fruits from mixed pollinations compared with cross‐pollinations is probably due to ovule discounting caused by self‐fertilization. Moreover, germinability of seeds with developed embryos was lower in fruits from mixed than from cross‐pollinations, and the non‐viable seeds from mixed pollinations showed one‐third of the mass of those from cross‐pollinations.
• The great number of empty seeds, lower germinability, lower mass of non‐viable seeds, and higher variation in seed mass distribution in mixed pollinations, strongly suggests early‐acing inbreeding depression in putative selfed seeds. In this sense, LSI and inbreeding depression acting together probably constrain self‐fertilized seedling establishment in A. peregrinum.

     

Internal transport of alien and native plants by geese and ducks: an experimental study

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Temporal,but not spatial,changes in expression patterns of petal identity genes are associated with loss of papillate conical cells and the shift to bird pollination in Macaronesian Lotus (Leguminosae)

• In the generally bee‐pollinated genus Lotus a group of four species have evolved bird‐pollinated flowers. The floral changes in these species include altered petal orientation, shape and texture. In Lotus these characters are associated with dorsiventral petal identity, suggesting that shifts in the expression of dorsal identity genes may be involved in the evolution of bird pollination. Of particular interest is Lotus japonicus CYCLOIDEA 2 (LjCYC2), known to determine the presence of papillate conical cells on the dorsal petal in L. japonicus. Bird‐pollinated species are unusual in not having papillate conical cells on the dorsal petal.
• Using RT‐PCR at various stages of flower development, we determined the timing of expression in all petal types for the three putative petal identity genes (CYC‐like genes) in different species with contrasting floral morphology and pollination syndromes.
• In bird‐pollinated species the dorsal identity gene, LjCYC2, is not expressed at the floral stage when papillate conical cells are normally differentiating in bee‐pollinated species. In contrast, in bee‐pollinated species, LjCYC2 is expressed during conical cell development.
• Changes in the timing of expression of the above two genes are associated with modifications in petal growth and lateralisation of the dorsal and ventral petals in the bird‐pollinated species. This study indicates that changes in the timing, rather than spatial distribution, of expression likely contribute to the modifications of petal micromorphology and petal size during the transition from bee to bird pollination in Macaronesian Lotus species.

     

Unravelling the structure and function of the petal appendages in the tribe Schwenckieae (Solanaceae)

• The tribe Schwenckieae (Solanaceae) is characterised by the presence of appendages on the corolla, a diagnostic trait for the group. These appendages constitute a median distal projection of the three‐lobed petal and occur in the genera Melananthus and Schwenckia but are absent in Heteranthia.
• We investigated the micromorphology and anatomical structure of the appendages and lateral petal lobes of Schwenckia americana (two varieties), S. angustifolia, S. curviflora and S. novaveneciana, and Melananthus fasciculatus. We also performed histochemical tests to determine if the appendages are involved in the production of volatiles, acting as a fragrance secretory structure (osmophore).
• The appendages have a uniseriate epidermis, whose cells store phenolics and lipids. The parenchyma is starch‐rich just prior to anthesis in all species studied. The sensory test and anatomical analyses identified scent‐secreting tissues, not only in the appendages, but also in the lateral petal lobes, whose cells are papillose with a sculptured surface. The α‐naphthol p‐phenylenediamine (NADI) reaction detected volatile (essential oils) compounds in S. americana var. americana and S. americana var. angustifolia.
• We demonstrated the secretory tissues and the production of lipids in the corolla appendages of Schwenckia and Melananthus, which indicate their osmogenic function and probable scent emission to attract pollinators.

     

Seed handling behaviours of native and invasive seed‐dispersing ants differentially influence seedling emergence in an introduced plant

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